Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Ao Chen¹, Yidi Sun², Ying Lei³, Chao Li⁴, Sha Liao⁵, Juan Meng⁴, Yiqin Bai⁶, Zhen Liu⁷, Zhifeng Liang⁴, Zhiyong Zhu⁸, Nini Yuan⁴, Hao Yang⁴, Zihan Wu⁹, Feng Lin⁸, Kexin Wang⁴, Mei Li⁸, Shuzhen Zhang⁴, Meisong Yang⁸, Tianyi Fei⁴, Zhenkun Zhuang¹⁰, Yiming Huang⁴, Yong Zhang¹⁰, Yuanfang Xu⁴, Luman Cui⁸, Ruiyi Zhang⁴, Lei Han⁸, Xing Sun⁴, Bichao Chen⁸, Wenjiao Li⁸, Baoqian Huangfu¹⁰, Kailong Ma⁸, Jianyun Ma⁷, Zhao Li⁸, Yikun Lin⁴, He Wang⁴, Yanqing Zhong⁴, Huifang Zhang⁴, Qian Yu⁴, Yaqian Wang⁴, Xing Liu⁸, Jian Peng⁸, Chuanyu Liu⁸, Wei Chen⁸, Wentao Pan⁹, Yingjie An⁴, Shihui Xia⁴, Yanbing Lu⁴, Mingli Wang⁴, Xinxiang Song⁴, Shuai Liu⁸, Zhifeng Wang⁸, Chun Gong¹¹, Xin Huang⁸, Yue Yuan⁸, Yun Zhao⁴, Qinwen Chai⁴, Xing Tan⁴, Jianfeng Liu⁴, Mingyuan Zheng⁴, Shengkang Li¹², Yaling Huang⁸, Yan Hong⁸, Zirui Huang⁸, Min Li⁸, Mengmeng Jin⁴, Yan Li⁴, Hui Zhang⁴, Suhong Sun⁴, Li Gao⁷, Yinqi Bai⁸, Mengnan Cheng⁸, Guohai Hu¹³, Shiping Liu³, Bo Wang¹³, Bin Xiang⁷, Shuting Li⁴, Huanhuan Li⁴, Mengni Chen⁴, Shiwen Wang⁴, Minglong Li⁴, Weibin Liu⁸, Xin Liu⁸, Qian Zhao⁸, Michael Lisby¹⁴, Jing Wang⁸, Jiao Fang⁴, Yun Lin⁸, Qing Xie⁸, Zhen Liu¹⁵, Jie He⁴, Huatai Xu⁶, Wei Huang⁴, Jan Mulder¹⁶, Huanming Yang⁸, Yangang Sun⁴, Mathias Uhlen¹⁶, Muming Poo¹⁵, Jian Wang¹¹, Jianhua Yao¹⁷, Wu Wei¹⁸, Yuxiang Li¹⁹, Zhiming Shen²⁰, Longqi Liu²¹, Zhiyong Liu²², Xun Xu²³, Chengyu Li²⁴

Affiliations

¹ BGI-Shenzhen, Shenzhen 518103, China; Department of Biology, University of Copenhagen, Copenhagen 2200, Denmark; BGI Research-Southwest, BGI, Chongqing 401329, China; JFL-BGI STOmics Center, Jinfeng Laboratory, Chongqing 401329, China.
² Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China. Electronic address: ydsun@ion.ac.cn.
³ BGI-Shenzhen, Shenzhen 518103, China; BGI-Hangzhou, Hangzhou 310012, China.
⁴ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
⁵ BGI-Shenzhen, Shenzhen 518103, China; BGI Research-Southwest, BGI, Chongqing 401329, China; JFL-BGI STOmics Center, Jinfeng Laboratory, Chongqing 401329, China.
⁶ Lingang Laboratory, Shanghai 200031, China.
⁷ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
⁸ BGI-Shenzhen, Shenzhen 518103, China.
⁹ Tencent AI Lab, Shenzhen 518057, China.
¹⁰ BGI-Shenzhen, Shenzhen 518103, China; School of Biology and Biological Engineering, South China University of Technology, Guangzhou 510006, China.
¹¹ BGI-Shenzhen, Shenzhen 518103, China; China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China.
¹² BGI-Shenzhen, Shenzhen 518103, China; Guangdong Bigdata Engineering Technology Research Center for Life Sciences, Shenzhen 518083, China.
¹³ China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China.
¹⁴ Department of Biology, University of Copenhagen, Copenhagen 2200, Denmark.
¹⁵ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China.
¹⁶ Department of Protein Science, Science for Life Laboratory, KTH-Royal Institute of Technology, Stockholm 17121, Sweden; Department of Neuroscience, Karolinska Institute, Stockholm 17177, Sweden.
¹⁷ Tencent AI Lab, Shenzhen 518057, China. Electronic address: jianhuayao@tencent.com.
¹⁸ Lingang Laboratory, Shanghai 200031, China; CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China. Electronic address: wuwei@lglab.ac.cn.
¹⁹ BGI-Shenzhen, Shenzhen 518103, China; BGI Research-Wuhan, BGI, Wuhan 430074, China. Electronic address: liyuxiang@genomics.cn.
²⁰ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China. Electronic address: zmshen@ion.ac.cn.
²¹ BGI-Shenzhen, Shenzhen 518103, China; BGI-Hangzhou, Hangzhou 310012, China. Electronic address: liulongqi@genomics.cn.
²² Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China. Electronic address: zhiyongliu@ion.ac.cn.
²³ BGI-Shenzhen, Shenzhen 518103, China; Guangdong Provincial Key Laboratory of Genome Read and Write, Shenzhen 518120, China. Electronic address: xuxun@genomics.cn.
²⁴ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China; School of Future Technology, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: tonylicy@lglab.ac.cn.

PMID: 37442136
DOI: 10.1016/j.cell.2023.06.009

Free article

Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Ao Chen et al. Cell. 2023.

Free article

. 2023 Aug 17;186(17):3726-3743.e24.

doi: 10.1016/j.cell.2023.06.009. Epub 2023 Jul 12.

Authors

Affiliations

¹ BGI-Shenzhen, Shenzhen 518103, China; Department of Biology, University of Copenhagen, Copenhagen 2200, Denmark; BGI Research-Southwest, BGI, Chongqing 401329, China; JFL-BGI STOmics Center, Jinfeng Laboratory, Chongqing 401329, China.
² Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China. Electronic address: ydsun@ion.ac.cn.
³ BGI-Shenzhen, Shenzhen 518103, China; BGI-Hangzhou, Hangzhou 310012, China.
⁴ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
⁵ BGI-Shenzhen, Shenzhen 518103, China; BGI Research-Southwest, BGI, Chongqing 401329, China; JFL-BGI STOmics Center, Jinfeng Laboratory, Chongqing 401329, China.
⁶ Lingang Laboratory, Shanghai 200031, China.
⁷ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
⁸ BGI-Shenzhen, Shenzhen 518103, China.
⁹ Tencent AI Lab, Shenzhen 518057, China.
¹⁰ BGI-Shenzhen, Shenzhen 518103, China; School of Biology and Biological Engineering, South China University of Technology, Guangzhou 510006, China.
¹¹ BGI-Shenzhen, Shenzhen 518103, China; China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China.
¹² BGI-Shenzhen, Shenzhen 518103, China; Guangdong Bigdata Engineering Technology Research Center for Life Sciences, Shenzhen 518083, China.
¹³ China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China.
¹⁴ Department of Biology, University of Copenhagen, Copenhagen 2200, Denmark.
¹⁵ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China.
¹⁶ Department of Protein Science, Science for Life Laboratory, KTH-Royal Institute of Technology, Stockholm 17121, Sweden; Department of Neuroscience, Karolinska Institute, Stockholm 17177, Sweden.
¹⁷ Tencent AI Lab, Shenzhen 518057, China. Electronic address: jianhuayao@tencent.com.
¹⁸ Lingang Laboratory, Shanghai 200031, China; CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China. Electronic address: wuwei@lglab.ac.cn.
¹⁹ BGI-Shenzhen, Shenzhen 518103, China; BGI Research-Wuhan, BGI, Wuhan 430074, China. Electronic address: liyuxiang@genomics.cn.
²⁰ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China. Electronic address: zmshen@ion.ac.cn.
²¹ BGI-Shenzhen, Shenzhen 518103, China; BGI-Hangzhou, Hangzhou 310012, China. Electronic address: liulongqi@genomics.cn.
²² Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China. Electronic address: zhiyongliu@ion.ac.cn.
²³ BGI-Shenzhen, Shenzhen 518103, China; Guangdong Provincial Key Laboratory of Genome Read and Write, Shenzhen 518120, China. Electronic address: xuxun@genomics.cn.
²⁴ Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 201602, China; School of Future Technology, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: tonylicy@lglab.ac.cn.

PMID: 37442136
DOI: 10.1016/j.cell.2023.06.009

Abstract

Elucidating the cellular organization of the cerebral cortex is critical for understanding brain structure and function. Using large-scale single-nucleus RNA sequencing and spatial transcriptomic analysis of 143 macaque cortical regions, we obtained a comprehensive atlas of 264 transcriptome-defined cortical cell types and mapped their spatial distribution across the entire cortex. We characterized the cortical layer and region preferences of glutamatergic, GABAergic, and non-neuronal cell types, as well as regional differences in cell-type composition and neighborhood complexity. Notably, we discovered a relationship between the regional distribution of various cell types and the region's hierarchical level in the visual and somatosensory systems. Cross-species comparison of transcriptomic data from human, macaque, and mouse cortices further revealed primate-specific cell types that are enriched in layer 4, with their marker genes expressed in a region-dependent manner. Our data provide a cellular and molecular basis for understanding the evolution, development, aging, and pathogenesis of the primate brain.

Keywords: cell-type organization; hierarchy; macaque cortex; single-cell; spatial transcriptome.

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Conflict of interest statement

Declaration of interests Stereo-seq is covered in pending patents. BGI employees hold company stock.

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Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Affiliations

Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Authors

Affiliations

Abstract

Conflict of interest statement

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